Alkhala_Hübener_ Porembski _2011 - Microalgae Trapped by Carnivorous Bladderworts - Utricularia

Plant Div. Evol. Vol. 129/2, 125–138 E Published online February 2011

© 2011 E. SchweizerbartÕsche Verlagsbuchhandlung, Stuttgart, Germany www.schweizerbart.deDOI: 10.1127/1869-6155/2011/0129-0037 1869-6155/2011/0129-0037 $ 03.50

Received January 22, 2010, in revised form July 7, 2010, accepted July 9, 2010

Microalgae trapped by carnivorous bladderworts (Utricularia, Lentibulariaceae): analysis, attributes and structure of the microalgae trapped

By Imad Aldeen Alkhalaf, Thomas Hübener and Stefan Porembski

With 8 figures and 3 tables

Abstract

Alkhalaf, I.A., Hübener, T. & Porembski, S.: Microalgae trapped by carnivorous bladderworts (Utric-ularia, Lentibulariaceae): analysis, attributes and structure of the microalgae trapped. — Plant Div. Evol. 129: 125–138. 2011. — ISSN 1869-6155.

Utricularia species capture small prey in traps. The prey spectrum of aquatic Utricularia species in-cludes a large variety of organisms (e.g. copepods, cladocerans, crustacea, rotifers, algae). This study focuses on selected attributes (species richness, density, biovolume, C and N contents) of microalgae captured inside the traps of aquatic Utricularia spp.. A total of 850 traps of four aquatic bladderwort species (Utricularia australis, U. foliosa, U. gibba and U. vulgaris) from tropical (Ivory Coast) and temperate (Canada, Germany) regions has been investigated concerning the algae captured. In total, 302 microalgal taxa have been identified with Bacillariophyceae, Chlorophyceae and Charophyceae being most species rich. The number of microalgae species captured was different among the Utricu-laria spp. It was relatively low inside the traps of U. gibba and U. foliosa from tropical Africa, with the greatest species diversity observed within the Charophyceae (Desmidiaceae). The highest mi-croalgae density, biovolume, C and N contents were observed within the traps of U. gibba/IC. There are considerable differences in the amount and composition of algae trapped among the Utricularia spiecies. The amount of microalgae captured does not relate to trap size parameters (length, height and volume).

Keywords: Utricularia, bladderworts, microalgae, carnivory, nutrients, phytogeography.

Introduction

Carnivorous plants have developed numerous adaptations in order to attract, trap and digest their prey (mainly insects) for obtaining essential nutrients such as nitrogen and phosphorus (cf Barthlott et al. 2004). For certain carnivorous plants information on prey spectra is available (e.g. Utricularia) but no comparative analyses exist with re-gard to the prey spectra between temperate and tropical regions.

Utricularia (Lentibulariaceae) comprises c. 220 species that are characterized by their unique bladder traps (for a survey on their morphology see Taylor 1989). Trap

126 I.A. Alkhalaf et al., Microalgae trapped bladderworts (Utricularia, Lentibulariaceae)

size usually ranges between 1–5 mm in length (Friday 1991) and most animals caught (e.g. ciliates, crustaceans) are small. Depending on the size and type of trap, the size of the captured prey animals can range from microscopic unicellular animals to verte-brates (Barthlott et al. 2007).

Remarkably, some aquatic species of Utricularia not only catch animal prey but also have been observed to trap microalgae (e.g. Bacillariophyceae, Chlorophyceae) with their suction traps. Recently (Mette et al. 2000, Díaz-Olarte et al. 2007, Peroutka, et al. 2008) the importance of the vegetarian diet of aquatic Utricularia species has been investigated in more detail. It could be shown that in Germany a large number of microalgae are trapped that might contribute to the nutritive supply (e.g. nitrogen) of bladderworts (Alkhalaf et al. 2009).

Here we report for the first time on the results of analysis and attributes of the cy-anobacteria and eukaryotic microalgae (in the following paper both labelled as ‘mi-croalgae’ or in case of multiple replication also ‘algae’) trapped by aquatic species of Utricularia from differential geographical regions in order to get first insights about possible region specific differences. Moreover, the C and N content of microalgae captured by Utricularia traps was examined.

Material and methods

The following species of Utricularia have been studied:

Utricularia species labelled as locality of sampling

U. australis R. Br U. australis/GER Retschow, Northeast Germany U. vulgaris L. U. vulgaris/GER Retschow, Northeast Germany U. vulgaris L. U. vulgaris/CAN Rocky Mountains Region, CanadaU. foliosa L. U. foliosa/IC Comoé National Park, Ivory CoastU. gibba L. U. gibba/IC Comoé National Park, Ivory Coast

All samples were taken between July 2006 and August 2007. The chemical characters of the water-bodies in northeast Germany are summarized in Table 1. Chlorophyceae is the most species-rich group of the examinated Northgerman water-bodies and it was dominated by colony-forming species such as Scenedesmus spp. Kirchneriella spp. Monoraphidium spp. and Dictyosphaerium spp.. The Canadian lake is oligotrophic, acid and relatively shallow with a maximum depth of 2.5 m. U. folisa/IC and U. gibba/IC were collected from a shallow, oligotrophic marsh. However, other chemical properties of the tropical and Canadian lakes are not available in this paper.

The samples were preserved in 4% formalin solution for further inspection. In the laboratory, the plants were divided into small segments with 2–3 traps per segment. A total of 850 traps was exam-ined (U. australis/GER = 227 traps, U. foliosa/IC = 100 traps, U. gibba/IC = 100 traps, U. vulgaris/CAN = 105 traps, and U. vulgaris/GER = 318 traps) to determine the microalgae captured. Microal-gae adherent to the outer trap wall was removed by washing with distilled water.

The traps were cut and opened with a thin insect needle, the trap length was measured under a light microscope as the greatest length from stalk end to trap-door end (Friday 1991) using the program AnalySIS for windows. The traps were subdivided into eight size classes between 400 und 4200 µm. In order to calculate the volume the traps were divided into two parts (front as a cone, back as a half sphere); the finally volume was calculated as the sum of both. The trap content was examined under a light microscope (Zeiss Axioplan) and the microalgae or elements of them were subsequently deter-

I.A. Alkhalaf et al., Microalgae trapped bladderworts (Utricularia, Lentibulariaceae) 127

mined and identified to the lowest taxonomic level possible. Algae biovolume was calculated for each taxon using the formula for the geometric shape (Edler 1979, Reynolds & Bellinger 1992, Pohlmann & Friedrich 2001, Vadrucci et al. 2007). The total algal biovolume was calculated by the addition of the biovolume of all species present (abundance x volume).

Based on the total algal biovolume, carbon and nitrogen content of the various species of microal-gae were determined using the conversion described by Menden-Deuer & Lessard (2000).

Results

Species composition

Microalgae assemblages in 850 traps of 4 aquatic Utricularia species were determined (Fig. 1). In total, 302 taxa out of 82 genera belonging to 10 orders could be identified. Most species rich were Bacillariophyceae (31% of the trapped algae, 21 genera, 95 taxa) and Chlorophyceae (31%, 35 genera, 94 taxa) followed by Charophyceae (Desmi-diaceae) (28%, 13 genera, 84 taxa), cyanobacteria (7%, 10 genera, 21 taxa), Eugleno-phyceae (2%, 2 genera, 5 taxa) and Dinophyceae (1%, 1 genus, 3 taxa).

A relatively high number of microalgae was found in traps of U. vulgaris/GER (58 genera, dominant: Kirchneriella, Monoraphidium, Scenedesmus), 179 species. In traps of U. australis/GER 58 genera/150 species were recorded. Dominant genera were Ank-istrodesmus, Pediastrum and Scenedesmus. In traps of U. vulgaris/CAN 28 genera (dominant: Cosmarium, Eunotia and Pinnularia) with at all 78 species have been found. Lowest numbers were found in traps of U. foliosa/IC 24 genera/45 spp. (domi-nant: Cosmarium, Scenedesmus, Staurastrum) and U. gibba 11 genera/31 spp. (domi-nant: Closterium, Cosmarium, Staurastrum).

Concerning their relative abundance of all individuals, Chlorophyceae were domi-nant in traps of U. australis/GER (90%), U. vulgaris/GER (66%) and U. foliosa/IC (41%). In traps of U. gibba/IC Desmidiaceae is dominant (83%) whereas in U. vul-garis/CAN-traps Bacillariophyceae such as Eunotia spp. is preponderant (58%). Planktonic cyanobacteria, such as Microcystis spp., Chroococcus spp. were most

Table 1. Mean values of chemical variables measured between July 2006 and August 2007.

Kettle hole number

Mean parameter K. 1 K. 2 K. 3 K. 4

Total-P (µg L-1) 0.18 0.08 0.42 0.06Orthophosphate (µg L-1) 0.08 0.02 0.05 0.02Total-N (µg L-1) 3.38 4.21 6.97 1.46NH4-N (µg L-1) 0.17 0.12 0.19 0.08NO3 (µg L-1) 0.08 0.11 0.66 0.03NO2-N (µg L-1) 0.005 0.005 0.009 0.004pH 6.6 7.1 6.5 6.7


prominent in traps of U. vulgaris/GER (14%) and were completely absent from traps of U. foliosa/IC and U. gibba/IC. Euglenophyceae were found in traps of all species except U. vulgaris/CAN. Dinophyceae could only be recorded in traps of U. australis/GER and U. vulgaris/GER.

Fig. 1. Species richness (total number of microalgae taxa found) in the traps of Utricularia spp.

Fig. 2. The percentage composition of the main algal groups recorded in the examined traps of four species of Utricularia.


Density and biovolume of microalgae

There were obvious differences in the quantitative and qualitative composition of the microalgae found in traps of the Utricularia species studied (Fig. 2, 3). The average number of individuals per trap varied between the Utricularia species and ranged from 10 individuals per trap of U. vulgaris/CAN to 67 individuals per trap of U. australis/GER. The value reached 48 individuals per trap of U. vulgaris/GER, 16 and 14 indi-viduals per trap were by U. foliosa/IC and U. gibba/IC, respectively.

Fig. 3. Population density of captured microalgae in one mL trap volume.

Fig. 4. Total algae biovolume of the traps of Utricularia spp.


Algae density in the traps ranged from 2.5 ×103 cells mL-1 (U. vulgaris/CAN) to 92.8 × 103 cells mL-1 (U. gibba/IC). For details on all species studied see Fig. 3.

Total algae biovolumes ranged from 0.0236 mm3 mL-1 (U. vulgaris/GER) to 2.3 mm3

mL-1 in U. gibba/IC (Fig. 4). In Fig. 5 details are presented on the biovolume of indi-vidual groups of the microalgae. In general, Charophyceae and Chlorophyceae reach the highest values. Euglenophyceae and Dinophyceae contributed a relatively minor amount of biovolume.

Carbon and nitrogen content of microalgae

The capture of algae leads to an input of e.g. C and N into the traps of Utricularia de-pending on the quality and quantity of prey. The average total C and N that were po-tentially made available per trap differed widely between individual species of Utricu-laria (see Fig. 6). The C and N contents of captured algae in traps of U. gibba from Ivory Coast were about four times higher than in the traps of U. vulgaris from both Germany and Canada. The most interesting is that the both U. vulgaris/GER and U. vulgaris/CAN have similar average values of C and N content per trap.

The Desmidiaceae contributed most C and N in the traps of U. foliosa/IC, U. gibba/IC and U. vulgaris/CAN while Chlorophyceae were most important C and N contribu-tors in traps of investigated Utricularia species in Germany (U. australis and U. vul-garis).

Fig. 5. Biovolume percentage of microalgae taxa.


Trap volume

The average volume of traps varied widely between individual traps of Utricularia species. It was lowest in U. gibba/IC (0.15 ± 0.08 mm3) and highest in U. vulgaris/CAN (4 ± 3.4 mm3) and U. foliosa/IC (4 ± 1.1 mm3). The difference of traps volume among the Utricularia species was significant (F = 78.3, p < 0.05).

The percentage ratio of total biovolume of microalgae captured/volume of traps ranged between 0.002% and 0.23%. The highest value was recorded for U. gibba/IC (0.23%) and the lowest value was 0.002% for both U. vulgaris from Canada and Ger-many. The percentage ratio reached a value of 0.009% and 0.003% for the other spe-cies from Ivory Coast (U. australis and U. foliosa), respectively (Fig. 7).

Fig. 6. Mean contents (ng) of (A) carbon and (B) nitrogen of captured microalgae per trap.

B

A


Fig. 7. Relation between total volume of traps (mm3) and total biovolume of captured microalgae (mm3).

Table 2. Relation between the length (µm) and height (µm) of the examined traps.

Parameter U. vulgaris/ U. foliosa/ U. gibba/ U. vulgaris/ U. australis/ CAN IC IC GER GER

Mean ± SD (L) 2286 ± 570 2335 ± 241 852 ±146 1975 ± 706 1668 ± 472Max (L) 4100 2755 1162 3558 2800Min (L) 1358 1257 547 460 670Mean ± SD (H) 1792 ± 510 2116 ± 223 643 ±107 1636 ± 528 1387 ± 439Max (H) 3700 2581 908 3200 2423Min (H) 1024 950 387 147 143p-value (L*H) ≤ 0.05 ≤ 0.05 ≤ 0.05 ≤ 0.05 ≤ 0.05r2-value (L*H) 0.896 0.707 0.763 0.853 0.839

Trap size and frequency of microalgae trapped

The length of Utricularia traps is generally larger than their height. The maximum (4100 µm) and minimum (460 µm) values of the trap length were detected in U. vul-garis/GER. The height ranged between 143 µm in U. australis/GER and 3700 µm in U. vulgaris/CAN (Table 2). The linear relationships between trap length and height are correlated positively in the traps of all examined species.

In general, with the exception of U. vulgaris/GER, there was no significant relation-ship between trap size (length, height, volume) and the amount of microalgae captured. The frequency distribution of the total number of captured algae varied with trap length and height (Fig. 8) of the individual Utricularia species. In nearly all species of Utric-ularia, traps that captured the largest number of microalgae ranged from 0.7 to 8.0 mm3 in volume.


Fig. 8. Frequency distributions of microalgae individuals across the (A) trap length (B) trap high and (C) trap value.

A

B

C


Discussion

The discussion focuses on the differences in microalgae spectra between the Utricu-laria species studied and on the amount of potential nutrients made available from the microalgae trapped.

Species composition and microalgae spectra

The microalgae composition in the traps of Utricularia was similar to those described in previous studies (Goebel 1891, Lemmermann 1914, Hegner 1926, Schumacher 1960, Mosto 1979, Wagner & Mshigeni 1986, Mette et al. 2000, Gordon & Pacheco 2007, Díaz-Olarte et al. 2007, Peroutka et al. 2008, Sirová et al. 2009).

The differences in trapped microalgae diversity and composition might be a result of differences in the general algae composition at the growth sites of the Utricularia species studied (Zamora 1995) what could be due to particular physico-chemical fea-tures (Guisande et al. 2004, Peroutka et al. 2008). The qualitative and quantitative of plankton composition is related to water temperature, light conditions, nutrient levels and chemical changes (Fott 1971, Gordon & Pacheco 2007). Mette et al. (2000) showed that aquatic bladderwort species in different German habitats do not capture their prey objects selectively but in dependence on the available prey community and the prey composition differs with regard to species and quantity.

It was also noted that only algae and not zooplankton were presented in the exam-ined traps of Utricularia spp.. Gordon & Pacheco (2007) and Peroutka et al. (2008) found that U. gibba and other aquatic Utricularia species contain more than 50% of the examined traps algal taxa without zooplankton. Peroutka et al. (2008) further sug-gested that the number of trapped animals and algae did not correlate. The Euglena spp. is trapped under controlled conditions without zooplankton presence (Jobson et al. 2000).

Utricularia australis and U. vulgaris from Germany shared a considerable number of trapped microalgae taxa (115) what is possibly due to the close neighbourhood of the sampling sites. Eleven microalgae taxa (5 Bacillariophyceae, 4 Charophyceae, 2 Chlorophyceae) occurred in traps of both German and Canadian Utricularia species.

The microalgae spectra of U. foliosa and U. gibba from Ivory Coast differed con-siderably and only 6 taxa (out of 45 and 31 taxa recorded in traps of U. foliosa and U. gibba, respectively) were in common (5 Charophyceae, 1 Euglenophyceae) what could be the result of a larger distance between the sampling sites. Only very few microalgae taxa (e.g. Pediastrum duplex, P. tetras, Ankistrodesmus gracilis) have been found in traps of both temperate and tropical Utricularia species. Only one species (Cosmarium laeve, Charophyceae) was observed in the traps of all species is examined. Some of the identified algal taxa in the analyzed traps, like Ankistrodesmus falcatus, Dictyospha-erium pulchellum and Scenedesmus quadricauda, are cosmopolitan. They are found in almost all water types and characterized by ubiquitous forms (Fott 1971).

This study as well as previous studies could not resolve the trapping process of the microalgae and whether they are digested by Utricularia spp.. Mette et al. (2000) ob-served the algae trapped and found that they use the traps as a habitat in which they


photosynthesize and reproduce. The traps may serve the algae as protection from pred-ators (Wagner and Mshigeni, 1986). Desmidiales may favour the lower pH found in-side the traps of Utricularia (Sirová et al. 2003, 2009) and Euglenphyceae may prefer the trap environment due to high concentrations of organic nutrients (Palmer 1969). Utricularia spp. possibly confine living organisms not only to absorb nitrogen and phosphorous, also for the CO2 produced through respiratory activity of community inside the traps (Gordon & Pacheco 2007).

We could not find a clear relationship between trap dimensions (length, height, volume) and the amount of microalgae trapped what agrees with the results obtained by other authors (Adamec 2009, Jobson & Morris 2001, Reifenrath et al. 2006, San-abria-Aranda et al. 2006, Slack 2000). However, another important point is that the amount of algae inside the examined traps of U. vulgaris/GER and U. australis/GER showed significant relationships (p ≤ 0.05) to the pH, the conductivity as well as the P- and N-concentrations of the water-bodies (data not shown). So our results do not support the hypothesis of Peroutka et al. (2008) that no correlation among pH and percentage of algae exists (Table 3).

Our results on trap size agree well with previous studies (Adamec 2009, Guiral & Rougier 2007, Jobson & Morris 2001, Reifenrath et al. 2006, Sanabria-Aranda et al. 2006, Slack 2000, Taylor 1989). Friday (1991) calculated the mean volume values of traps of U. vulgaris. They ranged from 0.11 to 8.45 µL and from 1 to 4 mm in length. These calculations are in agreement with our results. The trap size of Utricularia cf. gibba from Brazil varied from 0.2 to 1.7 µL in volume and from 0.7 to 1.5 mm in length (Walker 2004).

The shape and size of Utricularia traps differ considerably between species and are often used as an aid for species identification. Some species also show variation within populations (Juniper et al. 1989). Guisande et al. (2000) suggested that the size and number of the traps changing according to the prevailing conditions of the habitat. The differences of trap size do not reflect differences in age of traps (Friday 1991) or stag-es in the growth of individual traps (Wallace 1975). In our Study, we found U. gibba/IC has the smallest traps, but the amount of trapped algae in the traps was high. The possible reason for this is that the abundance and quality of algae in their surrounding water were higher than other habitats. The capture potential depends on the quality, quantity or the availability of the organisms and on the environmental conditions in the

Table 3. Relation between the length, height and volume of the examined traps and the number of microalgae individuals.

U. vulgaris/ U. foliosa/ U. gibba/ U. vulgaris/ U. australis/ CAN IC IC GER GER

(L*n) p-value 0.850 0.341 0.660 0.000 0.654 r2-value 0.000 0.009 0.002 0.096 0.001(H*n) p-value 0.861 0.038 0.212 0.002 0.213 r2-value 0.000 0.043 0.016 0.03 0.007(V*n) p-value 0.959 0.230 0.557 0.001 0.154 r2-value 0.000 0.015 0.004 0.037 0.009


habitats where the plants grow (Kurbatova & Yershov 2009, Zamora 1995). It is un-questionable that any variation on plankton communities will have an effect on prey spectra (Zamora 1995). Gordon & Pacheco (2007) have shown that the prey composi-tion reflects possibly the plankton biodiversity outside the traps.

Biovolume and C and N contents of microalgae

Differences in the biovolume of the microalgae trapped are due to different prey spectra with U. gibba/IC ranking first (mainly trapping Charophyceae with relatively large biovolume). Generally, the C and N contents of the microalgae trapped are com-paratively low (maximum 39 and 8 ng C and N per trap). The total nitrogen content of captured zooplankton inside the traps of U. australis/GER and U. vulgaris/GER ranged from 105 to 346 ng N/trap and between 134 and 396 ng N/trap, respectively (own un-published data) and is thus considerably higher.

The total nitrogen content of Utricularia tissue depends on its age (Friday & Quarmby 1994). Tissue concentrations of N and P are usually below 2% and 0.1%, respectively (Ellison, 2006). Carnivorous plants are able to extract 10–87% of their seasonal N content from animal prey (see Ellison & Gotelli 2001).

Moeller (1980) and Troxler & Richards (2009) have shown that tissue of U. purpu-rea is relatively rich in nitrogen (2.9% and 1.9% dry weight, respectively), but poor in P (0.084% and 0.057%, respectively). Other aquatic species such as U. foliosa have a N-content of 2.26% and the C:N ratio was 23 (Troxler & Richards 2009) with traps of U. foliosa having a very high C:N ratio between 12 and 37 (Guisande et al. 2004).

Tissue contents of nutrients of U. australis senescent shoot segments depended sig-nificantly on the trophic level of habitats (Adamec 2008). The existence of microalgae inside the examined traps does not imply that the captured algae is used as nutrition for Utricularia. It is still not clear to what extent the nitrogen of the captured microalgae is used by Utricularia.

The higher number of microalgae taxa in traps of temperate bladderworts could be due to the higher number of traps examined from temperate Utricularia species. 45 algal genera were identified inside the traps of four aquatic Utricularia spp. from Aus-tria (Peroutka et al. 2008). Sirová et al. (2009) have found more algal species inside the traps of U. foliosa (126) and U. purpurea (132) from the Czech Republic.

Lewis (1978) reported that tropical lakes tend to have lower algae diversity than temperate lakes. Kalff & Watson (1986) have found that the phytoplankton species of tropical lakes do not, in large measure, differ from those in the temperate zone. The differences in the taxonomic composition of the microalgae trapped by Utricularia thus does not seem to be a function of latitude but seems to be rather the consequence of stochastic events.

Acknowledgements

We thank Prof. Dr. W. Barthlott (Bonn), Prof Dr. D. Hessen (Oslo), Dr. P. Kosiba (Wroclaw), Dr. L. Adamec (Třeboň), Dr. R. Heerkloß, Dr. D. Goetze, S. Adler (all Rostock) and N. Hobbhahn (Calgary) for providing material and for valuable discussions.


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Addresses of the authors: Imad Aldeen Alkhalaf, Thomas Hübener, Stefan Porembski, Universität Rostock, Institut für Bio-

wissenschaften, Allgemeine und Spezielle Botanik, Wismarsche Str. 8, 18051 Rostock, Germany. Corresponding author, e-mail: [email protected]

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Alkhala_Hübener_ Porembski _2011 - Microalgae Trapped by Carnivorous Bladderworts - Utricularia